Redox-Responsive Transcription Factor 1 (RRFT1) Is Involved in Extracellular ATP-Regulated Arabidopsis thaliana Seedling Growth

Abstract

Extracellular adenosine triphosphate (eATP) is an apoplastic signaling molecule that plays an essential role in the growth and development of plants. Arabidopsis seedlings have been reported to respond to eATP; however, the downstream signaling components are still not well understood. In this study, we report that an ethylene-responsive factor, Redox-Responsive Transcription Factor 1 (RRTF1), is involved in eATP-regulated Arabidopsis thaliana seedling growth. Exogenous adenosine triphosphate inhibited green seedling root growth and induced hypocotyl bending of etiolated seedlings. RRTF1 loss-of-function mutant (rrtf1) seedlings showed decreased responses to eATP, while its complementation or overexpression led to recovered or increased eATP responsiveness. RRTF1 was expressed rapidly after eATP stimulation and then migrated into the nuclei of root tip cells. eATP-induced auxin accumulation in root tip or hypocotyl cells was impaired in rrtf1. Chromatin immunoprecipitation and high-throughput sequencing results indicated that eATP induced some genes related to cell growth and development in wild type but not in rrtf1 cells. These results suggest that RRTF1 may be involved in eATP signaling by regulating functional gene expression and cell metabolism in Arabidopsis seedlings.

Insights into Plant Extracellular ATP Signaling Revealed by the Discovery of an ATP-Regulated Transcription Factor

“…Secondly, the recent hypothesis that apoplast signalling represents a mechanism for collective decision-making in similar fashion to quorum-sensing bacteria identified eATP signalling as a classic example (Chivasa and Goodman, 2019). This study (Zhu et al, 2020) has now raised the possibility of the existence of additional receptor protein(s), which will certainly be subject to future research in addressing these fundamental questions. Extracellular ATP signals via an as yet unknown plasma membrane receptor (which is not DORN1) to activate second messengers, such as Ca 2+ ions, reactive oxygen species (ROS), nitric oxide (NO), and phosphatidic acid.…”

“…These physiological responses to ATP are thought to arise from altered distribution of auxin. Zhu et al (2020) have now demonstrated that the ATP effects on auxin spatial profiles and root growth are mediated via RRTF1. ATP-induced spread of auxin distribution beyond the quiescent zone (to cortical and epidermal cells) seen in wildtype roots is abolished in loss-of-function rrtf1 mutants.…”

“…In this issue, Zhu et al (2020) investigated the role of a stress-responsive transcription factor in mediating the effects of ATP on Arabidopsis roots. The Arabidopsis gene coding for Redox-Responsive Transcription Factor 1 (RRTF1) is rapidly stimulated (within minutes) on exposure to exogenous ATP.…”

“…However, secretion of ATP in healthy and actively growing tissues (Kim et al, 2006) does not fit with such an interpretation. Identification of RRTF1 as an ATP-responsive factor with a suite of putative target genes involved in cell division, cell expansion, and gravitropic growth (Zhu et al, 2020) suggests that eATP has a fundamental function in growth processes that is above its role as a danger signal (Figure 1). Perhaps the link established by Zhu et al (2020) between RRTF1 and genes required for active growth might explain why an energy molecule (ATP) abundant in actively-growing sink tissues (such as root tips) is an appropriate switch to turn on this form of signalling.…”

“…In this model, the plasma membrane demarcates the intracellular ATP (iATP) pool used for energy from the eATP pool used for signalling. Diagram based on the findings of Zhu et al (2020).…”